Background: Kirtland’s warblers are the rarest songbird species in North America, rarity due in part to a reliance on early successional Jack Pine forests. Habitat loss due to fire suppression led to population declines to fewer than 200 males during the 1970s. Subsequent conservation management has allowed the species to recover to over 1700 males by 2010. In this study, we directly examine the impact that low population sizes have had on genetic variation in Kirtland’s warblers. We compare the molecular variation of samples collected in Oscoda County, Michigan across three time periods: 1903–1912, 1929–1955 and 2008–2009. Results: In a hierarchical rarified sample of 20 genes and one time period, allelic richness was highest in 1903–1912 sample (AR = 5.96), followed by the 1929–1955 sample (AR = 5.74), and was lowest in the 2008–2009 sample (AR = 5.54). Heterozygosity measures were not different between the 1929–1955 and 2008–2009 samples, but were lower in the 1903–1912 sample. Under some models, a genetic bottleneck signature was present in the 1929–1955 and 2008–2009 samples but not in the 1903–1912 sample. Conclusions: We suggest that these temporal genetic patterns are the result of the declining Kirtland’s warbler population compressing into available habitat and a consequence of existing at low numbers for several decades.